OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons (original) (raw)

• Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683 (1982).
  Article CAS PubMed Google Scholar
• Eichenbaum, H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109–120 (2004).
  Article CAS PubMed Google Scholar
• Murray, A.J. et al. Parvalbumin-positive CA1 interneurons are required for spatial working, but not for reference memory. Nat. Neurosci. 14, 297–299 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Korotkova, T., Fuchs, E.C., Ponomarenko, A., von Engelhardt, J. & Monyer, H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations and working memory. Neuron 68, 557–569 (2010).
  Article CAS PubMed Google Scholar
• Freund, T.F. & Buzsaki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996).
  Article CAS PubMed Google Scholar
• Somogyi, P. & Klausberger, T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. (Lond.) 562, 9–26 (2005).
  Article CAS Google Scholar
• Ascoli, G.A. et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557–568 (2008).
  Article CAS PubMed Google Scholar
• Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154–165 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Maccaferri, G. & McBain, C.J. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15, 137–145 (1995).
  Article CAS PubMed Google Scholar
• Tort, A.B., Rotstein, H.G., Dugladze, T., Gloveli, T. & Kopell, N.J. On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc. Natl. Acad. Sci. USA 104, 13490–13495 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Gloveli, T. et al. Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc. Natl. Acad. Sci. USA 102, 13295–13300 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Rotstein, H.G. et al. Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. J. Neurophysiol. 94, 1509–1518 (2005).
  Article PubMed Google Scholar
• Wulff, P. et al. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. USA 106, 3561–3566 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Nakauchi, S., Brennan, R.J., Boulter, J. & Sumikawa, K. Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2* nicotinic ACh receptors. Eur. J. Neurosci. 25, 2666–2681 (2007).
  Article PubMed Google Scholar
• Cutsuridis, V., Cobb, S. & Graham, B.P. Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20, 423–446 (2010).
  CAS PubMed Google Scholar
• Hasselmo, M.E. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351–359 (1999).
  Article CAS PubMed Google Scholar
• Ishii, K., Wong, J.K. & Sumikawa, K. Comparison of alpha2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice. J. Comp. Neurol. 493, 241–260 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Jia, Y., Yamazaki, Y., Nakauchi, S. & Sumikawa, K. Alpha2 nicotine receptors function as a molecular switch to continuously excite a subset of interneurons in rat hippocampal circuits. Eur. J. Neurosci. 29, 1588–1603 (2009).
  Article PubMed PubMed Central Google Scholar
• Jia, Y., Yamazaki, Y., Nakauchi, S., Ito, K. & Sumikawa, K. Nicotine facilitates long-term potentiation induction in oriens-lacunosum moleculare cells via Ca2+ entry through non-alpha7 nicotinic acetylcholine receptors. Eur. J. Neurosci. 31, 463–476 (2010).
  Article PubMed PubMed Central Google Scholar
• Maccaferri, G. & McBain, C.J. The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J. Physiol. (Lond.) 497, 119–130 (1996).
  Article CAS Google Scholar
• Palmer, L.M. & Stuart, G.J. Site of action potential initiation in layer 5 pyramidal neurons. J. Neurosci. 26, 1854–1863 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Tong, Q., Ye, C.-P., Jones, J.E., Elmquist, J.K. & Lowell, B.B. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nat. Neurosci. 11, 998–1000 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kee, M.Z., Wuskell, J.P., Loew, L.M., Augustine, G.J. & Sekino, Y. Imaging activity of neuronal populations with new long-wavelength voltage-sensitive dyes. Brain Cell Biol. 36, 157–172 (2008).
  Article PubMed Google Scholar
• Cardin, J.A. et al. Targeted optogenetic stimulation and recording of neurons in vivo using cell type–specific expression of Channelrhodopsin-2. Nat. Protoc. 5, 247–254 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Maccaferri, G. & Dingledine, R. Control of feedforward dendritic inhibition by NMDA receptor–dependent spike timing in hippocampal interneurons. J. Neurosci. 22, 5462–5472 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159–1163 (2001).
  Article CAS PubMed Google Scholar
• Maccaferri, G., Roberts, J.D., Szucs, P., Cottingham, C.A. & Somogyi, P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. (Lond.) 524, 91–116 (2000).
  Article CAS Google Scholar
• Tu, B., Gu, Z., Shen, J.X., Lamb, P.W. & Yakel, J.L. Characterization of a nicotine-sensitive neuronal population in rat entorhinal cortex. J. Neurosci. 29, 10436–10448 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Blasco-Ibáñez, J.M. & Freund, T.F. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur. J. Neurosci. 7, 2170–2180 (1995).
  Article PubMed Google Scholar
• Minneci, F. et al. Signaling properties of stratum oriens interneurons in the hippocampus of transgenic mice expressing EGFP in a subset of somatostatin-containing cells. Hippocampus 17, 538–553 (2007).
  Article CAS PubMed Google Scholar
• Veruki, M.L., Oltedal, L. & Hartveit, E. Electrical coupling and passive membrane properties of AII amacrine cells. J. Neurophysiol. 103, 1456–1466 (2010).
  Article PubMed Google Scholar
• Gulyás, A.I., Gorcs, T.J. & Freund, T.F. Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37, 31–44 (1990).
  Article PubMed Google Scholar
• Gulyás, A.I. et al. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J. Neurosci. 30, 15134–15145 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Klausberger, T. et al. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat. Neurosci. 7, 41–47 (2004).
  Article CAS PubMed Google Scholar
• Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Fuchs, E.C. et al. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53, 591–604 (2007).
  Article CAS PubMed Google Scholar
• Cardin, J.A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lovett-Barron, M. et al. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 15, 423–430 (2012).
  Article CAS PubMed Google Scholar
• Elfant, D., Pál, B.Z., Emptage, N. & Capogna, M. Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur. J. Neurosci. 27, 104–113 (2008).
  Article PubMed Google Scholar
• Kim, S., Guzman, S.J., Hu, H. & Jonas, P. Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons. Nat. Neurosci. 15, 600–606 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Colom, L.V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. J. Neurochem. 96, 609–623 (2006).
  Article CAS PubMed Google Scholar
• Davis, J.A. & Gould, T.J. Associative learning, the hippocampus, and nicotine addiction. Curr. Drug Abuse Rev. 1, 9–19 (2008).
  Article CAS PubMed Google Scholar
• Lynch, M.A. Long-term potentiation and memory. Physiol. Rev. 84, 87–136 (2004).
  Article CAS PubMed Google Scholar
• Dugladze, T. et al. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc. Natl. Acad. Sci. USA 104, 17530–17535 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Neymotin, S.A. et al. Ketamine disrupts theta modulation of gamma in a computer model of hippocampus. J. Neurosci. 31, 11733–11743 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Stanley, E.M., Fadel, J.R. & Mott, D.D. Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol. Aging 33, 431 e1–13 (2012).
  Article PubMed CAS Google Scholar
• Franklin, K.B.J. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates 3rd edn. (Elsevier, 2007).
• Marshall, V.M., Allison, J., Templeton, T. & Foote, S.J. Generation of BAC transgenic mice. Methods Mol. Biol. 256, 159–182 (2004).
  CAS PubMed Google Scholar
• Leão, R.N., Tan, H.M. & Fisahn, A. Kv7/KCNQ channels control action potential phasing of pyramidal neurons during hippocampal gamma oscillations in vitro. J. Neurosci. 29, 13353–13364 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Zhou, W.L., Yan, P., Wuskell, J.P., Loew, L.M. & Antic, S.D. Intracellular long-wavelength voltage-sensitive dyes for studying the dynamics of action potentials in axons and thin dendrites. J. Neurosci. Methods 164, 225–239 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Leão, R.N. et al. A voltage-sensitive dye–based assay for the identification of differentiated neurons derived from embryonic neural stem cell cultures. PLoS ONE 5, e13833 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Leão, R.N., Colom, L.V., Borgius, L., Kiehn, O. & Fisahn, A. Medial septal dysfunction by Abeta-induced KCNQ channel-block in glutamatergic neurons. Neurobiol. Aging 33, 2046–2061 (2012).
  Article PubMed CAS Google Scholar
• Gezelius, H., Wallen-Mackenzie, A., Enjin, A., Lagerstrom, M. & Kullander, K. Role of glutamate in locomotor rhythm generating neuronal circuitry. J. Physiol. Paris 100, 297–303 (2006).
  Article CAS PubMed Google Scholar
• Enjin, A. et al. Identification of novel spinal cholinergic genetic subtypes disclose Chodl and Pitx2 as markers for fast motor neurons and partition cells. J. Comp. Neurol. 518, 2284–2304 (2010).
  Article CAS PubMed Google Scholar